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Dietary factors affecting hindgut protein fermentation in broilers: a review

Published online by Cambridge University Press:  10 March 2015

S.N. QAISRANI ,
M.M. VAN KRIMPEN ,
R.P. KWAKKEL ,
M.W.A. VERSTEGEN  and
W.H. HENDRIKS
S.N. QAISRANI*
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, NL-6700 AH Wageningen, The Netherlands Department of Animal Nutrition, University of Veterinary and Animal Sciences, Lahore, Pakistan
M.M. VAN KRIMPEN
Affiliation:
Wageningen UR Livestock Research, PO Box 65, NL-8200 AB Lelystad, The Netherlands
R.P. KWAKKEL
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, NL-6700 AH Wageningen, The Netherlands
M.W.A. VERSTEGEN
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, NL-6700 AH Wageningen, The Netherlands
W.H. HENDRIKS
Affiliation:
Animal Nutrition Group, Department of Animal Sciences, Wageningen University, PO Box 338, NL-6700 AH Wageningen, The Netherlands
*
Corresponding author: [email protected]
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Abstract

High growth rates in modern-day broilers require diets concentrated in digestible protein and energy. In addition to affecting feed conversion efficiency, it is important to prevent surplus dietary protein because of greater amounts of undigested protein entering the hindgut that may be fermented by the resident microbiota. The latter may result in increased formation of a wide range of protein-derived compounds including ammonia, amines, indoles and phenols, in addition to secondary products (lactate, succinate) and gases such as methane, hydrogen and carbon dioxide. In poultry, studies have shown the presence of protein fermentation products such as biogenic amines and branched chain fatty acids (BCFA) in the ileal and caecal digesta. The production and metabolism of nitrogenous waste products (as a result of protein fermentation) such as uric acid and ammonia may lead to a burden on the organism and cause additional energy losses. Although biogenic amines are important for normal gut development, greater concentrations may cause gizzard erosion, mortality and depressed growth rate in broilers. A decrease in indigestible protein reduces hindgut protein fermentation. In broilers, feeding diets with coarse particles (between 600 to 900 μm) and/or using feed additives, such as pre- and probiotics and organic acids, especially butyric acid, may improve protein digestion, thereby, potentially reducing hindgut protein fermentation. Studies are therefore needed to determine the extent and importance of hindgut protein fermentation on performance and gut health in broilers.

Keywords

gut healthprotein fermentationhindgutbroilersfeeding strategyorganic acids
Type
Reviews
Information
World's Poultry Science Journal , Volume 71 , Issue 1 , March 2015 , pp. 139 - 160
Copyright
Copyright © World's Poultry Science Association 2015 

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References

ABDL-RAHMAN, M., SALEH, S.Y., AMAL, A.Z. and ABD EL-HAMID SAFAA, S. (2011) Growth performance, caecal fermentation and blood biochemistry of rabbits fed diet supplemented with urea-bentonite combination. Journal of Agricultural Science 3: 14-21.Google Scholar
ADIL, S., BANDAY, T., BHAT, G.A., MIR, M.S. and REHMAN, M. (2010) Effect of dietary supplementation of organic acids on performance, intestinal histomorphology, and serum biochemistry of broiler chicken. Veterinary Medicine International 10: 4061-4067.Google Scholar
ADIL, S., BANDAY, T., BHAT, G.A., SALAHUDDIN, M., RAQUIB, M. and SHANAZ, S. (2011) Response of broiler chicken to dietary supplementation of organic acids. Journal of Central European Agriculture 12: 498-508.Google Scholar
ALLISON, C. and MACFARLANE, G.T. (1989) Influence of pH, nutrient availability, and growth rate on amine production by Bacteroides fragilis and Clostridium perfringens. Applied and Environmental Microbiology 55: 2894-2898.Google Scholar
AMERAH, A.M., RAVINDRAN, V., LENTLE, R.G. and THOMAS, D.G. (2007) Feed particle size: Implications on the digestion and performance of poultry. World's Poultry Science Journal 63: 439-455.Google Scholar
AMERAH, A.M., RAVINDRAN, V., LENTLE, R.G. and THOMAS, D.G. (2008) Influence of feed particle size on the performance, energy utilisation, digestive tract development, and digesta parameters of broiler starters fed wheat- and corn-based diets. Poultry Science 87: 2320-2328.Google Scholar
ANTONGIOVANNI, M., BUCCIONI, A., PETACCHI, F., LEESON, S., MINIERI, S., MARTINI, A. and CECCHI, R. (2009) Butyric acid glycerides in the diet of broiler chickens: effects on gut histology and carcass composition. Italian Journal of Animal Science 6: 19-26.Google Scholar
ANUGWA, F.O., VAREL, V.H., DICKSON, J.S., POND, W.G. and KROOK, L.P. (1989) Effects of dietary fiber and protein concentration on growth, feed efficiency, visceral organ weights and large intestine microbial populations of swine. Journal of Nutrition 119: 879-886.Google Scholar
APAJALAHTI, J., KETTUNEN, A. and GRAHAM, H. (2004) Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World's Poultry Science Journal 60: 223-232.Google Scholar
BALL, R.O. and AHERNE, F.X. (1987) Influence of dietary nutrient density, level of feed intake and weaning age on young pigs. II. Apparent nutrient digestibility and incidence and severity of diarrhea. Canadian Journal of Animal Science 67: 1105-1115.Google Scholar
BARNES, D.M., KIRBY, Y.K. and OLIVER, K.G. (2001) Effects of biogenic amines on growth and the incidence of proventricular lesions in broiler chickens. Poultry Science 80: 906-911.Google Scholar
BARNES, E.M., MEAD, G.C., BARNUML, D.A. and HARRY, E.G. (1972) The intestinal flora of the chicken in the period 2 to 6 weeks of age, with particular reference to the anaerobic bacteria. British Poultry Science 13: 311-326.Google Scholar
BJERRUM, L., ENGBERG, R.M., LESER, T.D., JENSEN, B.B., FINSTER, K. and PEDERSEN, K. (2006) Microbial community composition of the ileum and caecum of broiler chickens as revealed by molecular and culture-based techniques. Poultry Science 85: 1151-1164.Google Scholar
BJERRUM, L., PEDERSEN, A.B. and ENGBERG, R.M. (2005) The influence of whole wheat feeding on salmonella infection and gut flora composition in broilers. Avian Diseases 49: 9-15.Google Scholar
BRITTON, R. and KREHBIEL, C. (1993) Nutrient metabolism by gut tissues. Journal of Dairy Science 76: 2125-2131.Google Scholar
BUWJOOM, T., YAMAUCHI, K., ERIKAWA, T. and GOTO, H. (2010) Histological intestinal alterations in chickens fed low protein diet. Journal of Animal Physiology and Animal Nutrition 94: 354-361.Google Scholar
CAO, B.H., KARASAWA, Y. and GUO, Y.M. (2005) Effects of green tea polyphenols and fructo-oligosaccharides in semi-purified diets on broilers’ performance and caecal microflora and their metabolites. Asian-Australasian Journal of Animal Sciences 18: 85-89.Google Scholar
CHAVEZ, C., COUFAL, C.D., CAREY, J.B., LACEY, R.E., BEIER, R.C. and ZAHN, J.A. (2004) The impact of supplemental dietary methionine sources on volatile compound concentrations in broiler excreta. Poultry Science 83: 901-910.Google Scholar
CHEN, K., GAO, J., LI, J., HUANG, Y., LUO, X. and ZHANG, T. (2012) Effects of probiotics and antibiotics on diversity and structure of intestinal microflora in broiler chickens. African Journal of Microbiology Research 6: 6612-6617.Google Scholar
CHEN, T.C. (2003) Effect of adding chicory fructans in feed on faecal and intestinal microflora and excreta volatile ammonia. International Journal of Poultry Science 2: 188-194.Google Scholar
CHOCT, M. (2009) Managing gut health through nutrition. British Poultry Science 50: 9-15.Google Scholar
CUMMINGS, J.H. (1983) Fermentation in the human large intestine: Evidence and implications for health. Lancet 1: 1206-1209.Google Scholar
CUMMINGS, J.H. and BINGHAM, S.A. (1987) Dietary fibre, fermentation and large bowel cancer. Cancer Surveys 6: 601-621.Google Scholar
CUMMINGS, J.H. and MACFARLANE, G.T. (2002) Gastrointestinal effects of prebiotics. British Journal of Nutrition 87: S145–S151.Google Scholar
CVB (Central Bureau for Livestock Feeding) (2007) Veevoedertabel 2007, Centraal Veevoederbureau, Lelystad, The Netherlands.Google Scholar
DAHIYA, J.P., HOEHLER, D., WILKIE, D.C., VAN KESSEL, A.G. and DREW, M.D. (2005) Dietary glycine concentration affects intestinal Clostridium perfringens and Lactobacilli populations in broiler chickens. Poultry Science 84: 1875-1885.Google Scholar
DALMASSO, G., NGUYEN, H.T., YAN, Y., CHARRIER-HISAMUDDIN, L., SITARAMAN, S.V. and MERLIN, D. (2008) Butyrate transcriptionally enhances peptide transporter PepT1 expression and activity. PLoS ONE 3: e2476.Google Scholar
DANICKE, S., VAHJEN, W., SIMON, O. and JEROCH, H. (1999) Effects of dietary fat type and xylanase supplementation to rye-based broiler diets on selected bacterial groups adhering to the intestinal epithelium. on transit time of feed, and on nutrient digestibility. Poultry Science 78: 1292-1299.Google Scholar
DE LANGE, L., ROMBOUTS, C. and ELFERINK, O.G. (2003) Practical application and advantages of using total digestible amino acids and undigestible crude protein to formulate broiler diets. World's Poultry Science Journal 59: 447-457.Google Scholar
DE PRETER, V., ARIJS, I., WINDEY, K., VANHOVE, W., VERMEIRE, S., SCHUIT, F., RUTGEERTS, P. and VERBEKE, K. (2012) Decreased mucosal sulphide detoxification is related to an impaired butyrate oxidation in ulcerative colitis. Inflammatory Bowel Diseases 18: 2371-2380.Google Scholar
DE PRETER, V., HAMER, H.M., WINDEY, K. and VERBEKE, K. (2011) The impact of pre- and/or probiotics on human colonic metabolism: Does it affect human health? Molecular Nutrition & Food Research 55: 46-57.Google Scholar
DREW, M.D., SYED, N.A., GOLDADE, B.G., LAARVELD, B. and VAN KESSEL, A.G. (2004) Effects of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens. Poultry Science 83: 414-420.Google Scholar
ELSDEN, S.R., HILTON, M.G. and WALLER, J.M. (1976) The end products of the metabolism of aromatic amino acids by Clostridia. Archives of Microbiology 107: 283-288.Google Scholar
ENGBERG, R.M., HEDEMANN, M.S., LESER, T.D. and JENSEN, B.B. (2000) Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers. Poultry Science 79: 1311-1319.Google Scholar
ENGBERG, R.M., HEDEMANN, M.S. and JENSEN, B.B. (2002) The influence of grinding and pelleting of feed on the microbial composition and activity in the digestive tract of broiler chickens. British Poultry Science 43: 569-579.Google Scholar
ENGBERG, R.M., HEDEMANN, M.S., STEENFELDT, S. and JENSEN, B.B. (2004) Influence of whole wheat and xylanase on broiler performance and microbial composition and activity in the digestive tract. Poultry Science 83: 925-938.Google Scholar
FABER, T.A., DILGER, R.N., HOPKINS, A.C., PRICE, N.P. and FAHEY, G.C. Jr (2012) The effects of a galactoglucomannan oligosaccharide-arabinoxylan (GGMO-AX) complex in broiler chicks challenged with Eimeria acervulina. Poultry Science 91: 1089-1096.Google Scholar
FASANO, A. and SHEA-DONOHUE, T. (2005) Mechanisms of disease: The role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nature Clinical Practice Gastroenterology and Hepatology 2: 416-422.Google Scholar
FERRELL, C.L. (1988) Contribution of visceral organs to animal energy expenditures. Journal of Animal Science 66: 23-34.Google Scholar
FOSSUM, O., SANDSTEDT, K. and ENGSTRÖM, B.E. (1988) Gizzard erosions as a cause of mortality in white leghorn chickens. Avian Pathology 17: 519-525.Google Scholar
GABRIEL, I., MALLET, S. and LECONTE, M. (2003) Differences in the digestive tract characteristics of broiler chickens fed on complete pelleted diet or on whole wheat added to pelleted protein concentrate. British Poultry Science 44: 283-290.Google Scholar
GABRIEL, I., MALLET, S. and SIBILLE, P. (2005) Digestive microflora of bird: factors of variation and consequences on bird. INRA Production Animales 18: 309-322.Google Scholar
GABRIEL, I., MALLET, S., LECONTE, M., FORT, G. and NACIRI, M. (2006) Effects of whole wheat feeding on the development of coccidial infection in broiler chickens until market age. Animal Feed Science and Technology 129: 279-303.Google Scholar
GABRIEL, I., MALLET, S., LECONTE, M., TRAVEL, A. and LALLES, J.P. (2008) Effects of whole wheat feeding on the development of the digestive tract of broiler chickens. Animal Feed Science and Technology 142: 144-162.Google Scholar
GALLAZZI, D., GIARDINI, A., MANGIAGALLI, M.G., MARELLI, S., FERRAZZI, V., ORSI, C. and CAVALCHINI, L.G. (2009) Effects of Lactobacillus acidophilus D2/CSL on laying hen performance. Italian Journal of Animal Science 7: 27-38.Google Scholar
GIBSON, G.R., PROBERT, H.M., LOO, J.V., RASTALL, R.A. and ROBERFROID, M.B. (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutrition Research Reviews 17: 259-275.Google Scholar
GILL, C.I. and ROWLAND, I.R. (2002) Diet and cancer: assessing the risk. British Journal of Nutrition 88: 73-87.Google Scholar
GUNAL, M., YAYLI, G., KAYA, O., KARAHAN, N. and SULAK, O. (2006) The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. International Journal of Poultry Science 5: 149-155.Google Scholar
GUO, F.C., WILLIAMS, B.A., KWAKKEL, R.P. and VERSTEGEN, M.W.A. (2003) In vitro fermentation characteristics of two mushroom species, an herb, and their polysaccharide fractions, using chicken caecal contents as inoculum. Poultry Science 82: 1608-1615.Google Scholar
HARRY, E.G., TUCKER, J.F. and LAURSEN JONES, A.P. (1975) The role of histamine and fish meal in the incidence of gizzard erosion and proventricular abnormalities in the fowl. British Poultry Science 16: 69-78.Google Scholar
HAVENSTEIN, G.B., FERKET, P.R. and QURESHI, M.A. (2003) Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82: 1509-1518.Google Scholar
HENDRIKS, W.H., VAN BAAL, J. and BOSCH, G. (2012) Ileal and faecal protein digestibility measurement in humans and other non-ruminants a comparative species view. British Journal of Nutrition 108: S247-257.Google Scholar
HEO, J.M., KIM, J.C., HANSEN, C.F., MULLAN, B.P., HAMPSON, D.J. and PLUSKE, J.R. (2009) Feeding a diet with decreased protein content reduces indices of protein fermentation and the incidence of postweaning diarrhea in weaned pigs challenged with an enterotoxigenic strain of Escherichia coli. Journal of Animal Science 87: 2833-2843.Google Scholar
HETLAND, H., SVIHUS, B., KROGDAHL and Å. (2003) Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. British Poultry Science 44: 275-282.Google Scholar
HOBBS, P.J., PAIN, B.F., KAY, R.M. and LEE, P.A. (1996) Reduction of odorous compounds in fresh pig slurry by dietary control of crude protein. Journal of the Science of Food and Agriculture 71: 508-514.Google Scholar
HTOO, J.K., ARAIZA, B.A., SAUER, W.C., RADEMACHER, M., ZHANG, Y., CERVANTES, M. and ZIJLSTRA, R.T. (2007) Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and caecal digesta of early-weaned pigs. Journal of Animal Science 85: 3303-3312.Google Scholar
HU, Z. and GUO, Y. (2007) Effects of dietary sodium butyrate supplementation on the intestinal morphological structure, absorptive function and gut flora in chickens. Animal Feed Science and Technology 132: 240-249.Google Scholar
JACOBS, C.M., UTTERBACK, P.L. and PARSONS, C.M. (2010) Effects of corn particle size on growth performance and nutrient utilisation in young chicks. Poultry Science 89: 539-544.Google Scholar
JANG, J.P. (2011) Comparative effect of achillea and butyric acid on performance, carcass traits and serum composition of broiler chickens. Annals of Biological Research 2: 469-473.Google Scholar
JEAUROND, E.A., RADEMACHER, M., PLUSKE, J.R., ZHU, C.H. and DE LANGE, C.F.M. (2008) Impact of feeding fermentable proteins and carbohydrates on growth performance, gut health and gastrointestinal function of newly weaned pigs. Canadian Journal of Animal Science 88: 271-281.Google Scholar
JERZSELE, A., SZEKER, K., CSIZINSZKY, R., GERE, E., JAKAB, C., MALLO, J. and GALFI, P. (2012) Efficacy of protected sodium butyrate, a protected blend of essential oils, their combination, and Bacillus amyloliquefaciens spore suspension against artificially induced necrotic enteritis in broilers. Poultry Science 91: 837-843.Google Scholar
JOZEFIAK, D., RUTKOWSKI, A., KACZMAREK, S., JENSEN, B.B., ENGBERG, R.M. and HØJBERG, O. (2010) Effect of β-glucanase and xylanase supplementation of barley-and rye-based diets on caecal microbiota of broiler chickens. British Poultry Science 51: 546-557.Google Scholar
KADIM, I.T., MOUGHAN, P.J. and RAVINDRAN, V. (2002) Ileal amino acid digestibility assay for the growing meat chicken-comparison of ileal and excreta amino acid digestibility in the chicken. British Poultry Science 43: 588-597.Google Scholar
KADOTA, H. and ISHIDA, Y. (1972) Production of volatile sulphur compounds by microorganisms. Annual Reviews in Microbiology 26: 127-138.Google Scholar
KHEMPAKA, S., CHITSATCHAPONG, C. and MOLEE, W. (2011) Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers. Journal of Applied Poultry Research 20: 1-11.Google Scholar
KIARIE, E., ROMERO, L.F. and NYACHOTI, C.M. (2013) The role of added feed enzymes in promoting gut health in swine and poultry. Nutrition Research Reviews 26: 71-88.Google Scholar
KIKUGAWA, K. and KATO, T. (1988) Formation of a mutagenic diazoquinone by interaction of phenol with nitrite. Food and Chemical Toxicology 26: 209-214.Google Scholar
KROČKO, M., ČANIGOVÁ, M., BEZEKOVÁ, J., LAVOVÁ, M., HAŠČÍK, P. and DUCKOVÁ, V. (2012) Effect of nutrition with propolis and bee pollen supplements on bacteria colonisation pattern in gastrointestinal tract of broiler chickens. Scientific Papers Animal Science and Biotechnologies 45: 63-67.Google Scholar
LARDY, H.A. and FELDOTT, G. (1950) The net utilisation of ammonium nitrogen by the growing rat. Journal of Biological Chemistry 186: 85-91.Google Scholar
LARQUÉ, E., SABATER-MOLINA, M. and ZAMORA, S. (2007) Biological significance of dietary polyamines. Nutrition 23: 87-95.Google Scholar
LAUDADIO, V., PASSANTINO, L., PERILLO, A., LOPRESTI, G., PASSANTINO, A., KHAN, R.U. and TUFARELLI, V. (2012) Productive performance and histological features of intestinal mucosa of broiler chickens fed different dietary protein levels. Poultry Science 91: 265-270.Google Scholar
LEESON, S., NAMKUNG, H., ANTONGIOVANNI, M. and LEE, E.H. (2005) Effect of butyric acid on the performance and carcass yield of broiler chickens. Poultry Science 84: 1418-1422.Google Scholar
LE POUL, E., LOISON, C., STRUYF, S., SPRINGAEL, J.Y., LANNOY, V., DECOBECQ, M.E., BREZILLON, S., DUPRIEZ, V., VASSART, G. and VAN DAMME, J. (2003) Functional characterisation of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. Journal of Biological Chemistry 278: 25481-25489.Google Scholar
LEWIS, S. and COCHRANE, S. (2007) Alteration of sulphate and hydrogen metabolism in the human colon by changing intestinal transit rate. American Journal of Gastroenterology 102: 624-633.Google Scholar
LU, J., IDRIS, U., HARMON, B., HOFACRE, C., MAURER, J.J. and LEE, M.D. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology 69: 6816-6824.Google Scholar
MACFARLANE, G.T., ALLISON, C., GIBSON, S.A. and CUMMINGS, J.H. (1988) Contribution of the microflora to proteolysis in the human large intestine. Journal of Applied Microbiology 64: 37-46.Google Scholar
MACFARLANE, G.T., GIBSON, G.R., BEATTY, E. and CUMMINGS, J.H. (1992) Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiology Letters 101: 81-88.Google Scholar
MACKIE, R.I., STROOT, P.G. and VAREL, V.H. (1998) Biochemical identification and biological origin of key odor components in livestock waste. Journal of Animal Science 76: 1331-1342.Google Scholar
MEYER, B., BESSEI, W., VAHJEN, W., ZENTEK, J. and HARLANDER-MATAUSCHEK, A. (2012) Dietary inclusion of feathers affects intestinal microbiota and microbial metabolites in growing Leghorn-type chickens. Poultry Science 91: 1506-1513.Google Scholar
MEYER, B., ZENTEK, J. and HARLANDER-MATAUSCHEK, A. (2013) Differences in intestinal microbial metabolites in laying hens with high and low levels of repetitive feather-pecking behavior. Physiology & Behavior 110: 96-101.Google Scholar
MIGNON-GRASTEAU, S., MULEY, N., BASTIANELLI, D., GOMEZ, J., PERON, A., SELLIER, N., MILLET, N., BESNARD, J., HALLOUIS, J. and CARRÉ, B. (2004) Heritability of digestibilities and divergent selection for digestion ability in growing chicks fed a wheat diet. Poultry Science 83: 860-867.Google Scholar
MOOKIAH, S., SIEO, C.C., RAMASAMY, K., ABDULLAH, N. and HO, Y.W. (2014) Effects of dietary prebiotics, probiotic and synbiotics on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens. Journal of the Science of Food and Agriculture 94: 341-348.Google Scholar
NAMROUD, N.F., SHIVAZAD, M. and ZAGHARI, M. (2008) Effects of fortifying low crude protein diet with crystalline amino acids on performance, blood ammonia level, and excreta characteristics of broiler chicks. Poultry Science 87: 2250-2258.Google Scholar
NAMROUD, N.F., SHIVAZAD, M. and ZAGHARI, M. (2009) Impact of dietary crude protein and amino acids status on performance and some excreta characteristics of broiler chicks during 10–28 days of age. Journal of Animal Physiology and Animal Nutrition 94: 280-286.Google Scholar
NIBA, A.T., BEAL, J.D., KUDI, A.C. and BROOKS, P.H. (2009) Bacterial fermentation in the gastrointestinal tract of non-ruminants: Influence of fermented feeds and fermentable carbohydrates. Tropical Animal Health and Production 41: 1393-1407.Google Scholar
NIR, I., HILLEL, R., PTICHI, I. and SHEFET, G. (1995) Effect of particle size on performance. 3. Grinding pelleting interactions. Poultry Science 74: 771-783.Google Scholar
NIR, I., HILLEL, R., SHEFET, G. and NITSAN, Z. (1994) Effect of grain particle size on performance. 2. Grain texture interactions. Poultry Science 73: 781-791.Google Scholar
NOLLET, H., DEPREZ, P., VAN DRIESSCHE, E. and MUYLLE, E. (1999) Protection of just weaned pigs against infection with F18+ Escherichia coli by non-immune plasma powder. Veterinary Microbiology 65: 37-45.Google Scholar
NOUSIAINEN, J. (1991) Comparative observations on selected probiotics and olaquindox as feed additives for piglets around weaning.2. Effect on villus length and crypt depth in the jejunum, caecum, and colon. Journal of Animal Physiology and Animal Nutrition 66: 224-230.Google Scholar
OPAPEJU, F.O., KRAUSE, D.O., PAYNE, R.L., RADEMACHER, M. and NYACHOTI, C.M. (2009) Effect of dietary protein level on growth performance, indicators of enteric health, and gastrointestinal microbial ecology of weaned pigs induced with postweaning colibacillosis. Journal of Animal Science 87: 2635-2643.Google Scholar
PACHECO, W.J., STARK, C.R., FERKET, P.R. and BRAKE, J. (2013) Evaluation of soybean meal source and particle size on broiler performance, nutrient digestibility, and gizzard development. Poultry Science 92: 2914-2922.Google Scholar
PANDA, A.K., RAO, S.V.R., RAJU, M.V.L.N. and SHYAM SUNDER, G. (2009) Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australasian Journal of Animal Sciences 22: 1026-1031.Google Scholar
RASTALL, R.A. (2004) Bacteria in the gut: friends and foes and how to alter the balance. Journal of Nutrition 134: 2022S-2026S.Google Scholar
RAVINDRAN, V., HEW, L.I., RAVINDRAN, G. and BRYDEN, W.L. (1999) A comparison of ileal digesta and excreta analysis for the determination of amino acid digestibility in food ingredients for poultry. British Poultry Science 40: 266-274.Google Scholar
REHMAN, H., BÖHM, J. and ZENTEK, J. (2008) Effects of differentially fermentable carbohydrates on the microbial fermentation profile of the gastrointestinal tract of broilers. Journal of Animal Physiology and Animal Nutrition 92: 471-480.Google Scholar
REHMAN, H.U., VAHJEN, W., AWAD, W.A. and ZENTEK, J. (2007) Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Archives of Animal Nutrition 61: 319-335.Google Scholar
REID, C.A. and HILLMAN, K. (1999) The effects of retrogradation and amylose/amylopectin ratio of starches on carbohydrate fermentation and microbial populations in the porcine colon. Animal Science 68: 503-510.Google Scholar
REIFFENSTEIN, R.J., HULBERT, W.C. and ROTH, S.H. (1992) Toxicology of hydrogen sulphide. Annual Review of Pharmacology and Toxicology 32: 109-134.Google Scholar
RICKE, S.C. (2003) Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poultry Science 82: 632-639.Google Scholar
RIST, V., BAUER, E., ECKLUND, M. and MOSENTHIN, R. (2011) Strategies to reduce fermentation of dietary protein in the pig's gastrointestinal tract. 20th International Scientific Symposium on Nutrition of Farm Animals' Zadravec-Erjavec Days', Radenci, 10-11 Nov 2011.Google Scholar
RUBIO, L.A., BRENES, A., SETIEN, I., DE LA ASUNCION, G., DURAN, N. and CUTULI, M.T. (1998) Lactobacilli counts in crop, ileum and caecum of growing broiler chickens fed on practical diets containing whole or dehulled sweet lupin (Lupinus angustifolius) seed meal. British Poultry Science 39: 354-359.Google Scholar
RUSSEK, M. (1970) Hepatic receptors and the neurophysiological mechanisms controlling feeding behavior. Neurosciences Research 4: 213-282.Google Scholar
SALMINEN, S., OUWEHAND, A.C. and ISOLAURI, E. (1998) Clinical applications of probiotic bacteria. International Dairy Journal 8: 563-572.Google Scholar
SALTER, D.N. and FULFORD, R.J. (1974) The influence of the gut microflora on the digestion of dietary and endogenous proteins: studies of the amino acid composition of the excreta of germ-free and conventional chicks. British Journal of Nutrition 32: 625-637.Google Scholar
SANDERS, M.E. (2008) Probiotics: definition, sources, selection, and uses. Clinical Infectious Diseases 46: S58-S61.Google Scholar
SCHIMKE, R.T. (1963) Studies on factors affecting the levels of urea cycle enzymes in rat liver. Journal of Biological Chemistry 238: 1012-1018.Google Scholar
SEBASTIAN, S., TOUCHBURN, S.P., CHAVEZ, E.R. and LAGUE, P.C. (1997) Apparent digestibility of protein and amino acids in broiler chickens fed a corn-soybean diet supplemented with microbial phytase. Poultry Science 76: 1760-1769.Google Scholar
SHIFRINE, M., ADLER, H.E. and OUSTERHOUT, I.E. (1960) The pathology of chicks fed histamine. Avian Diseases 4: 12-21.Google Scholar
SMITH, H.W. (1965) Observations on the flora of the alimentary tract of animals and factors affecting its composition. The Journal of Pathology and Bacteriology 89: 95-122.Google Scholar
SMITH, T. (1990) Effect of dietary putrescine on whole body growth and polyamine metabolism. Proceedings of the Society for Experimental Biology and Medicine 194: 332-336.Google Scholar
SMITS, C., VELDMAN, A., VERKADE, H. and BEYNEN, A. (1998) The inhibitory effect of carboxymethylcellulose with high viscosity on lipid absorption in broiler chickens coincides with reduced bile salt concentration and raised microbial numbers in the small intestine. Poultry Science 77: 1534-1539.Google Scholar
SVIHUS, B. (2011) The gizzard: function, influence of diet structure and effects on nutrient availability. World's Poultry Science Journal 67: 207-224.Google Scholar
SVIHUS, B., KLØVSTAD, K.H., PEREZ, V., ZIMONJA, O., SAHLSTRÖM, S., SCHÜLLER, R.B., JEKSRUD, W.K. and PRESTLØKKEN, E. (2004) Physical and nutritional effects of pelleting of broiler chicken diets made from wheat ground to different coarsenesses by the use of roller mill and hammer mill. Animal Feed Science and Technology 117: 281-293.Google Scholar
TAHERPOUR, K., MORAVEJ, H., SHIVAZAD, M., ADIBMORADI, M. and YAKHCHALI, B. (2009) Effects of dietary probiotic, prebiotic and butyric acid glycerides on performance and serum composition in broiler chickens. African Journal of Biotechnology 8: 2329-2334.Google Scholar
TAKAHASHI, M., KAMETAKA, M. and MITSUOKA, T. (1982) Influence of diets low in protein or lysine on the intestinal flora of chicks with reference to caecal contents. Journal of Nutritional Science and Vitaminology 28: 501-510.Google Scholar
TAZOE, H., OTOMO, Y., KAJI, I., TANAKA, R., KARAKI, S.I. and KUWAHARA, A. (2008) Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. Journal of Physiology and Pharmacology 59: 251-262.Google Scholar
TEN DOESCHATE, R.A.H.M., SCHEELE, C.W., SCHREURS, V.V.A.M. and VAN DER KLIS, J.D. (1993) Digestibility studies in broiler chickens: influence of genotype, age, sex and method of determination. British Poultry Science 34: 131-146.Google Scholar
TERADA, A., HARA, H., NAKAJYO, S., ICHIKAWA, H., HARA, Y., FUKAI, K., KOBAYASHI, Y. and MITSUOKA, T. (1993) Effect of supplements of tea polyphenols on the caeeal flora and caeeal metabolites of chicks. Microbial Ecology in Health and Disease 6: 3-9.Google Scholar
TERADA, A., HARA, H., SAKAMOTO, J., SATO, N., TAKAGI, S., MITSUOKA, T., MINO, R., HARA, K., FUJIMORI, I. and YAMADA, T. (1994) Effects of dietary supplementation with lactosucrose (4G-β-D-Galactosylsucrose) on caecal flora, caecal metabolites, and performance in broiler chickens. Poultry Science 73: 1663-1672.Google Scholar
TIIHONEN, K., KETTUNEN, H., BENTO, M.H.L., SAARINEN, M., LAHTINEN, S., OUWEHAND, A.C., SCHULZE, H. and RAUTONEN, N. (2010) The effect of feeding essential oils on broiler performance and gut microbiota. British Poultry Science 51: 381-392.Google Scholar
TOROK, V.A., HUGHES, R.J., MIKKELSEN, L.L., PEREZ-MALDONADO, R., BALDING, K., MC-ALPINE, R., PERCY, N.J. and OPHEL-KELLER, K. (2011) Identification and characterisation of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Applied and Environmental Microbiology 77: 5868-5878.Google Scholar
URLINGS, H.A.P., VAN LOGTESTIJN, J.G. and BIJKER, P.G.H. (1992) Slaughter by-products: problems, preliminary research and possible solutions. Veterinary Quarterly 14: 34-38.Google Scholar
VAN DER HOEVEN-HANGOOR, E., VAN DER VOSSEN, J.M.B.M., SCHUREN, F.H.J., VERSTEGEN, M.W.A., DE OLIVEIRA, J.E., MONTIJN, R.C. and HENDRIKS, W.H. (2013) Ileal microbiota composition of broilers fed various commercial diet compositions. Poultry Science 92: 2713-2723.Google Scholar
VAN DER WAAIJ, D. and NORD, C.E. (2000) Development and persistence of multi-resistance to antibiotics in bacteria; an analysis and a new approach to this urgent problem. International Journal of Antimicrobial Agents 16: 191-197.Google Scholar
VAN IMMERSEEL, F., BOYEN, F., GANTOIS, I., TIMBERMONT, L., BOHEZ, L., PASMANS, F., HAESEBROUCK, F. and DUCATELLE, R. (2005) Supplementation of coated butyric acid in the feed reduces colonisation and shedding of Salmonella in poultry. Poultry Science 84: 1851-1856.Google Scholar
VINCE, A.J. and BURRIDGE, S.M. (1980) Ammonia production by intestinal bacteria: the effects of lactose, lactulose and glucose. Journal of Medical Microbiology 13: 177-191.Google Scholar
WÄCHTERSHÄUSER, A. and STEIN, J. (2000) Rationale for the luminal provision of butyrate in intestinal diseases. European Journal of Nutrition 39: 164-171.Google Scholar
WANG, J.Y. and JOHNSON, L.R. (1990) Luminal polyamines stimulate repair of gastric mucosal stress ulcers. The American Journal of Physiology - Gastrointestinal and Liver Physiology 259: G584-G592.Google Scholar
WILKIE, D.C., VAN KESSEL, A.G., WHITE, L.J., LAARVELD, B. and DREW, M.D. (2005) Dietary amino acids affect intestinal Clostridium perfringens populations in broiler chickens. Canadian Journal of Animal Science 85: 185-193.Google Scholar
WILLIAMS, J., MALLET, S., LECONTE, M., LESSIRE, M. and GABRIEL, I. (2008) The effects of fructo-oligosaccharides or whole wheat on the performance and digestive tract of broiler chickens. British Poultry Science 49: 329-339.Google Scholar
WINDEY, K., DE PRETER, V. and VERBEKE, K. (2012) Relevance of protein fermentation to gut health. Molecular Nutrition and Food Research 56: 184-196.Google Scholar
WISE, M.G. and SIRAGUSA, G.R. (2007) Quantitative analysis of the intestinal bacterial community in one to three week old commercially reared broiler chickens fed conventional or antibiotic free vegetable based diets. Journal of Applied Microbiology 102: 1138-1149.Google Scholar
XIA, M.S., HU, C.H. and XU, Z.R. (2004) Effects of copper-bearing montmorillonite on growth performance, digestive enzyme activities, and intestinal microflora and morphology of male broilers. Poultry Science 83: 1868-1875.Google Scholar
XU, Z.R., HU, C.H., XIA, M.S., ZHAN, X.A. and WANG, M.Q. (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82: 1030-1036.Google Scholar
YASAR, S. (2003) Performance, gut size and ileal digesta viscosity of broiler chickens fed with a whole wheat added diet and the diets with different wheat particle sizes. International Journal of Poultry Science 2: 75-82.Google Scholar
ZUCCATO, E., VENTURI, M., DI LEO, G., COLOMBO, L., BERTOLO, C., DOLDI, S.B. and MUSSINI, E. (1993) Role of bile acids and metabolic activity of colonic bacteria in increased risk of colon cancer after cholecystectomy. Digestive Diseases and Sciences 38: 514-519.Google Scholar